Someone Like Me: Size-Assortative Pairing and Mating in an Amazonian Fish, Sailfin Tetra Crenuchus Spilurus
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RESEARCH ARTICLE Someone like me: Size-assortative pairing and mating in an Amazonian fish, sailfin tetra Crenuchus spilurus 1,2 1 1 Elio de Almeida BorghezanID *, Kalebe da Silva Pinto , Jansen Zuanon , Tiago Henrique da Silva Pires1 1 LaboratoÂrio de Ecologia Comportamental e EvolucËão, Instituto Nacional de Pesquisas da AmazoÃnia, Av. Andre ArauÂjo, Manaus, AM, Brazil, 2 Wildlife Research Center of Kyoto University, Sakyo-ku, Kyoto, Japan a1111111111 a1111111111 * [email protected] a1111111111 a1111111111 a1111111111 Abstract In the absence of constraints, preference for larger mates is expected to evolve, as larger individuals are typical of higher potential fitness. Large females are often more fecund and OPEN ACCESS carry larger eggs (which result in higher number and better quality of offspring), whereas Citation: Borghezan EdA, Pinto KdS, Zuanon J, large males usually have more conspicuous ornaments and are better at defending Pires THdS (2019) Someone like me: Size- resources. However, intrasexual competition can constrain the access to larger partners, assortative pairing and mating in an Amazonian especially when opportunities for mate takeover abound. Here we investigate the relation- fish, sailfin tetra Crenuchus spilurus. PLoS ONE 14 ship between individual's size and mate choice in relation to one's own size and their (9): e0222880. https://doi.org/10.1371/journal. pone.0222880 respective mate's size using the sailfin tetra, a sexually dimorphic Amazonian fish species. We show that ornaments of larger males are exponentially more conspicuous, and larger Editor: John A. B. Claydon, Institute of Marine Research, NORWAY females are more fecund and carry larger eggs. Contrary to expectation, neither males nor females associated for longer with the larger of two offered potential mates. Instead, Received: April 4, 2019 individuals of both genders chose opposite-sex individuals of similar sizes to themselves. Accepted: September 9, 2019 Additionally, similar-sized pairs were more likely to spawn than couples with higher size Published: September 27, 2019 asymmetries. Grounded on field observations, we propose that prudent choice should be Copyright: © 2019 Borghezan et al. This is an open particularly important in this system, since courtship is long (often taking several days), access article distributed under the terms of the which offers opportunities for mate takeover. Intrasexual competition, however, cannot Creative Commons Attribution License, which readily explain female choice for similar-sized males. We thus suggest that such preference permits unrestricted use, distribution, and reproduction in any medium, provided the original might be best explained by avoidance of filial cannibalism. author and source are credited. Data Availability Statement: All relevant data are in the paper and its Supporting Information files. Introduction Funding: We are thankful to CNPq for financial support to KSP and THSP, and for supporting JZ The correlation between traits of males and females in mated pairs is commonly observed with a productivity grant (#313183/2014-7) and for both in nature and in controlled experiments [1±5]. Known as assortative mating, this associa- providing EAB with a research grant (#313999/ tion can be based on a great variety of phenotypic characteristics [3]. Paired individuals can be 2017-1). EAB is grateful to MEXT similar in color [4,6], age [7,8], quality [9], or size [2,5]. Similarity in sizes of paired males and (Monbukagakusho #183957). THSP is thankful to FIXAM/FAPEAM (005/2018). We also thank CAPES females during mating is commonly reported and occurs in organisms ranging from earth- for providing scholarships and to Japan Science worms [10], insects [2,11], spiders [12], crustaceans [13], fishes [1], birds [14], and mammals and Technology Agency/Japan International [15]. PLOS ONE | https://doi.org/10.1371/journal.pone.0222880 September 27, 2019 1 / 19 Assortative mating in an Amazonian fish Cooperation Agency; Science and Technology Size-assortative mating may result from several processes, some not related to the active Research Partnership for Sustainable Development choice of partners [16,17]. Also, size assortative mating may be observed when individuals do for financing this study. This is contribution #60 of not prefer partners that are similar to themselves [1,5,16±18]. However, several cases have Projeto IgarapeÂs. The funders had no role in study design, data collection and analysis, decision to been reported in which individuals exert active preference for mating partners of similar sizes publish, or preparation of the manuscript. [2,12,13]. Due to their higher parental investments, females should choose mates from multiple Competing interests: The authors have declared that no competing interests exist. potential males [19,20]. Favoring larger males may yield multiple benefits to the choosing female, as larger males typically have higher competitive ability (or, resource holding poten- tial), often observed in their higher likelihood of winning dyadic encounters [17,21,22], in being better at maintaining larger and better territories [23,24], in successfully defending the offspring against conspecifics [25±27], or in being more capable of providing offspring with high-quality parental care, which include spending more time guarding the offspring, higher frequency of fanning and nest cleaning behavior [27,28]. Female choice may also be purely aes- thetic, as originally suggested by Charles Darwin [29,30]. Under purely aesthetic preference, larger males might be preferred, since they typically bear exponentially more conspicuous ornaments. Conversely, larger ornaments might exploit female choice for male size [31] and males with larger and more conspicuous ornaments may be favored by females, even at poten- tial viability cost for the bearer [32]. Additionally, because conspicuousness of ornaments often increases as males grow, so does the quality of signals emitted to females [33]. Males are expected to be selective for females when finding mates is not energetically demanding and when females vary highly in quality [34,35]. Male choice is also expected to occur when males contribute with a high investment to the mating partner and/or the off- spring [19,36], as they might be unavailable for mating for a long period, penalizing their potential reproductive rate [37], a pattern common in species with exclusive paternal care [19]. Since fecundity and egg size are often related to female body size [38,39], males often benefit from preferring larger females as mates [13,40±43]. Therefore, due to their high energetic expenditures in mating investment and parental care, both females and males are expected to choose larger mates in sexually dimorphic species with exclusive paternal care. However, when individuals of one or both sexes prefer to mate with larger (and higher quality) mates, preference for larger mate size might be constrained by intrasexual competition [2,5,13,44,45]. Under the scenario of strong competition for larger mates, smaller individuals might not be able to maintain high quality mates due to mate takeover [46±48], which may result in smaller or poor-quality individuals mating with smaller or lower quality mates [9,48]. When mate takeover is common, sexual selection should favor individuals that avoid investing time and effort in high quality mates they cannot maintain, resulting in preference for similar- sized partners [13,47,49,50]. This phenomenon has been termed prudent choice [51±53]. Because prudent mate choice occurs via takeover, it can be particularly important in species whose courtship or mate guarding until fertilization is long lasting [13,48,50]. Pairing of cou- ples can last for several days, or even weeks, in numerous organisms [54±57]. Under this sce- nario, opportunities are increased for larger males to potentially takeover larger females from smaller males. The sailfin tetra Crenuchus spilurus (Characiformes: Crenuchidae) is a sexually dimorphic and dichromatic Amazonian fish species (Fig 1). This species occurs in forest streams of semi- lentic and stable environmental conditions [56]. Males possess hypertrophied anal and dorsal fins that are conspicuously ornamented in red and yellow. Males spread the fins during a long and complex courtship behavior, which can last for several consecutive days [56]. Ornaments are also exhibited in male-male contests. Males exert exclusive paternal care for circa eight days, until the larvae detach from the nest substrate, whereas females seem not to play any important role in parental care [56]. During this period, males rarely leave the nest and refrain PLOS ONE | https://doi.org/10.1371/journal.pone.0222880 September 27, 2019 2 / 19 Assortative mating in an Amazonian fish Fig 1. Crenuchus spilurus individuals. Male above and female below. Note differences in size, shape and color of the anal and dorsal fins. https://doi.org/10.1371/journal.pone.0222880.g001 from feeding [56], which also decreases opportunities for courtship activity. Because males exert exclusive paternal care and females invest more energy per gamete, mutual mate choice could be expected in the sailfin tetra. Here we investigated the relationship of male and female body size with their respective conspicuousness and fecundity. Additionally, we asked whether males and females prefer larger partners or a preference for similar-sized partners was preva- lent. We addressed these questions by investigating male and female choice